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Ureaplasma Urealyticum and U. Parvum in Sexually Active Women Attending Public Health Clinics in Brazil

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Ureaplasma Urealyticum and U. Parvum in Sexually Active Women Attending Public Health Clinics in Brazil Epidemiol. Infect. (2017), 145, 2341–2351. © Cambridge University Press 2017 doi:10.1017/S0950268817001145 Ureaplasma urealyticum and U. parvum in sexually active women attending public health clinics in Brazil T. N. LOBÃO1,G.B.CAMPOS1,2,N.N.SELIS2,A.T.AMORIM1,S.G.SOUZA2, S. S. MAFRA2,L.S.PEREIRA2,D.B.DOSSANTOS3,T.B.FIGUEIREDO2, 1,2 1 L. M. MARQUES * AND J. TIMENETSKY 1 Instituto de Ciências Biomédicas, Departamento de Microbiologia, Universidade de São Paulo, Brazil 2 Instituto Multidisciplinar em Saúde, Núcleo de Tecnologia em Saúde, Universidade Federal da Bahia, Brazil 3 Centro de Ciências da Saúde, Universidade Federal do Recôncavo Baiano, Instituto de Ciências Biomédicas, Av. Professor Lineu Prestes, 1374. CEP 05508900, São Paulo, SP, Brazil Received 15 June 2016; Final revision 5 May 2017; Accepted 16 May 2017; first published online 22 June 2017 SUMMARY Ureaplasma urealyticum and U. parvum have been associated with genital infections. The purpose of this study was to detect the presence of ureaplasmas and other sexually transmitted infections in sexually active women from Brazil and relate these data to demographic and sexual health, and cytokines IL-6 and IL-1β. Samples of cervical swab of 302 women were examined at the Family Health Units in Vitória da Conquista. The frequency of detection by conventional PCR was 76·2% for Mollicutes. In qPCR, the frequency found was 16·6% for U. urealyticum and 60·6% U. parvum and the bacterial load of these microorganisms was not significantly associated with signs and symptoms of genital infection. The frequency found for Trichomonas vaginalis, Neisseria gonorrhoeae, Gardnerella vaginalis and Chlamydia trachomatis was 3·0%, 21·5%, 42·4% and 1·7%, respectively. Higher levels of IL-1β were associated with control women colonized by U. urealyticum and U. parvum. Increased levels of IL-6 were associated with women who exhibited U. parvum. Sexually active women, with more than one sexual partner in the last 3 months, living in a rural area were associated with increased odds of certain U. parvum serovar infection. Key words: Ureaplasma parvum, Ureaplasma urealyticum, urogenital infection. INTRODUCTION most of these infections are asymptomatic [2]. These Mollicutes Ureaplasma urealyticum and U. parvum are members of are also responsible for a variety of diseases the class Mollicutes, commonly referred to as mycoplas- and events such as non-gonococcal urethritis, endomet- ritis, pelvic inflammatory disease (PID), chorioamnio- mas. Both species are commensals of the human uro- genital tract. Infection rates as high as 40–80% in nitis, spontaneous abortion, premature birth, stillbirth women and 50% in men have been reported [1] and and neonatal bronchopulmonary dysplasia [3]. In the early days, U. urealyticum was divided into 14 serovars grouped into two biovars; biovar 1 com- * Author for correspondence: L. M. Marques, Instituto de Ciências posed of serovars 1, 3, 6, 14, while biovar 2 had 10 ser- Biomédicas, Departamento de Microbiologia, Universidade de São ovars 2, 4, 5, and 7–13, respectively. In 2002, biovars 1 Paulo, Brazil; Instituto Multidisciplinar em Saúde, Núcleo de Tecnologia em Saúde, Universidade Federal da Bahia, Brazil and 2 were renamed U. parvum and U. urealyticum, (Email: [email protected]) respectively. This reclassification was based on Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 27 Sep 2021 at 20:25:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268817001145 2342 T. N. Lobão and others differences based on genome size, 16S rRNA gene symptomatic women and 64 asymptomatic as a con- sequences, the 16S–23S rRNA intergenic region, trol group. Two women had missing observations enzyme polymorphisms, DNA–DNA hybridization, related to symptoms of genital infection, but kept in and differences in the multiple-banded antigen (mba) the overall prevalence calculations. The following genes [4]. women were excluded: sexually inactive women, The main characteristic of Ureaplasma spp. is their those using antibiotics in the last 3 months, pregnant ability to hydrolyze urea and release ammonia causing and HIV-positive women. The cervix of selected a local cytotoxic effect. In addition they also produce women was accessed using a sterile speculum, and IgA protease, urease, phospholipases A and C, and exudate was removed with a sterile swab. Two swabs hydrogen peroxide [5]. were collected from each woman. One was then placed The opportunistic role of mollicutes includes some in 5 ml of sterile transport medium [12] and stored at features of the innate immune response [6]. Ryckman −20 °C for molecular analysis. The other swab was et al. [7] observed that vaginal IL-1β, IL-6, and IL-8 then placed in a tube containing 1 ml phosphate- levels in pregnant were significantly higher in women buffer saline solution and stored at −70 °C for cyto- with any mycoplasma compared with those without. kines analysis. This may be related to bacterial surface molecules. A questionnaire that surveyed demographic details, Recognition of bacterial surface molecules by the obstetric and gynecologic history and knowledge innate immune system can trigger the production of about sexual behavior was administered. The ques- various proinflammatory cytokines from manifold tionnaire and the study were approved by the ethics cells, a surface component that causes inflammation committee of the Institute of Biomedical Sciences, [8–10]. Therefore it is possible to conclude that the University of São Paulo, Brazil. immune response to mollicutes is variable due the host and the antigenic mosaic and variation of molli- cutes. This may explain in part the potential role of DNA extraction Mollicutes in mammals to be excellent opportunistic Swabs were vigorously homogenized in a transport microorganisms that modulate the immune response medium and 1 ml of medium was used for the extraction. differently [11]. The DNA was extracted following the manufacturer’s When these Mollicutes are identified in clinical sam- instructions for Invitrogen Purelink Genomic DNA ples, U. parvum are observed to be more frequent than Kits (Invitrogen, São Paulo, SP, Brazil). U. parvum U. urealyticum. However, this distribution is contro- ATCC 27815 and U. urealyticum ATCC 33175 were versial due the antigenic variation or identification used as standard strains. The standard strains of methods of these Mollicutes. In this context, the aim Ureaplasma were the positive control, and UltraPure™ of the present study was to detect the prevalence of DNase/RNase-Free Distilled Water (Life Technology, U. urealyticum, U. parvum, U. parvum serovars, and Brazil) was the negative control for the PCR and qPCR other microorganisms of genital infections among methodology. The DNA of clinical samples and refer- sexually active women attending health clinics in ence strains were stored at −80 °C. Vitória da Conquista, Brazil. Conventional PCR and real-time TaqMan PCR METHODS This PCR procedure was used for detecting Mollicutes Endocervical samples (as a screening test), as described by van Kuppeveld This analytical cross-sectional study analyzed clinical et al. [13]. Positive samples for Mollicutes were analyzed samples from Vitória da Conquista city, the third lar- for Ureaplasma species. Primers and probes for U. urea- gest city of Bahia State, in the northeast of Brazil. The lyticum (UUureF/UUureR/ProbeUU) and U. parvum women included in the study attended a Brazilian (UPureF/UPureR/ProbeUP) were used for Real-time public health clinic, known as the ‘Unified Health PCR, as described by Cao et al. [14]. All reactions System’. Cervical swabs were obtained from 302 were performed in duplicate in a StepOnePlus real-time women consecutively attending a health clinic in PCR instrument (Applied Biosystems, Brazil). Vitória da Conquista, Brazil, from May to July 2011 Quantification was performed using an absolute quan- and in January 2012. Women with and without symp- tification technique, based on a predetermined standard toms of genital infection were studied, including 236 curve ranging from 107 to 10 microorganisms/μl. The Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.19, on 27 Sep 2021 at 20:25:30, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0950268817001145 Ureaplasma urealyticum and U. parvum in sexually active women attending public health clinics in Brazil 2343 data were acquired during the annealing step and ana- The real-time PCR detected 50 positive samples for lyzed using the StepOne Software 2.1 (Applied U. urealyticum and 183 for U. parvum. Co-infection Biosystems, Life Technologies Corporation). The Ct of both species was observed in 14 samples. U. parvum (threshold cycle) of the genome dilutions was plotted serovars 6 and 3/14 were the most frequent isolates in against the log number of genome copies and used as 64 (40·8%) and 62 (39·5%), respectively, followed by input to create the standard curve. Linear regression serovar 1 in 37 samples (23·6%). There were 27 analyses were then applied to calculate the r2 and samples that were cervical positive for U. parvum; slope values. Assuming 100% efficiency if the DNA however, they were negative for all four known template is doubled in each cycle, the PCR efficiency U. parvum serovars. was calculated as E = 10( − 1/slope) − 1, where E is We observed a prevalence of 42·4% (128/302) of G. PCR efficiency. The positive samples for U. parvum vaginalis infection, 21·5% (65/302) of N. gonorrhoeae, were then submitted to a specific conventional PCR to 3·0% (9/302) of T. vaginalis and 1·7% (5/302) of C. tra- detect serovars 1, 3, 6, and 14 of U. parvum [15]. chomatis. Among women with U. urealyticum, four were coinfected with T. vaginalis, nine with N. gonor- rhoeae, 25 with G.
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